Brain networks underlying tactile softness perception: A functional magnetic resonance imaging study.

Humans are adept at perceiving physical properties of an object through touch. Tangible object properties can be categorized into two types: macro-spatial properties, including shape and orientation; and material properties, such as roughness, softness, and temperature. Previous neuroimaging studies have shown that roughness and temperature are extracted at nodes of a network, such as that involving the parietal operculum and insula, which is different from the network engaged in processing macro-spatial properties. However, it is unclear whether other perceptual dimensions pertaining to material properties engage the same regions. Here, we conducted a functional magnetic resonance imaging study to test whether the parietal operculum and insula were involved in extracting tactually-perceived softness magnitude. Fifty-six healthy right-handed participants estimated perceived softness magnitude using their right middle finger. We presented three stimuli that had the same shape but different compliances. The force applied to the finger was manipulated at two levels. Classical mass-univariate analysis showed that activity in the parietal operculum, insula, and medial prefrontal cortex was positively associated with perceived softness magnitude, regardless of the applied force. Softness-related activity was stronger in the ventral striatum in the high-force condition than in the low-force condition. The multivariate voxel pattern analysis showed higher accuracy than chance levels and control regions in the parietal operculum/insula, postcentral gyrus, posterior parietal lobule, and middle occipital gyrus. These results indicate that a distributed set of the brain regions, including the parietal operculum and insula, is involved in representing perceived softness.

Cross-cultural similarity in relationship-specific social touching.

Many species use touching for reinforcing social structures, and particularly, non-human primates use social grooming for managing their social networks. However, it is still unclear how social touch contributes to the maintenance and reinforcement of human social networks. Human studies in Western cultures suggest that the body locations where touch is allowed are associated with the strength of the emotional bond between the person touched and the toucher. However, it is unknown to what extent this relationship is culturally universal and generalizes to non-Western cultures. Here, we compared relationship-specific, bodily touch allowance maps across one Western ( N = 386, UK) and one East Asian ( N = 255, Japan) country. In both cultures, the strength of the emotional bond was linearly associated with permissible touch area. However, Western participants experienced social touching as more pleasurable than Asian participants. These results indicate a similarity of emotional bonding via social touch between East Asian and Western cultures.

Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion.

Humans are adept at perceiving textures through touch. Previous neuroimaging studies have identified a distributed network of brain regions involved in the tactile perception of texture. However, it remains unclear how nodes in this network contribute to the tactile awareness of texture. To examine the hypothesis that such awareness involves the interaction of the primary somatosensory cortex with higher order cortices, we conducted a functional magnetic resonance imaging (fMRI) study utilizing the velvet hand illusion, in which an illusory velvet-like surface is perceived between the hands. Healthy participants were subjected to a strong illusion, a weak illusion, and tactile perception of real velvet. The strong illusion induced greater activation in the primary somatosensory cortex (S1) than the weak illusion, and increases in such activation were positively correlated with the strength of the illusion. Furthermore, both actual and illusory perception of velvet induced common activation in S1. Psychophysiological interaction (PPI) analysis revealed that the strength of the illusion modulated the functional connectivity of S1 with each of the following regions: the parietal operculum, superior parietal lobule, precentral gyrus, insula, and cerebellum. The present results indicate that S1 is associated with the conscious tactile perception of textures, which may be achieved via interactions with higher order somatosensory areas.

The brain network underlying the recognition of hand gestures in the blind: the supramodal role of the extrastriate body area.

The visual perception of others' body parts is critical for understanding and imitating their behavior. The visual cortex in humans includes the extrastriate body area (EBA), which is a large portion of the occipitotemporal cortex that is selectively responsive to visually perceived body parts. Previous neuroimaging studies showed that the EBA not only receives sensory inputs regarding others' body information but also receives kinesthetic feedback regarding one's own actions. This finding raised the possibility that the EBA could be formed via nonvisual sensory modalities. However, the effect of visual deprivation on the formation of the EBA has remained largely unknown. Here, we used fMRI to investigate the effect of vision loss on the development of the EBA. Blind and sighted human subjects performed equally well in a haptic-identification task involving three categories of objects (hand shapes, toy cars, and teapots). The superior part (i.e., the middle temporal gyrus and angular gyrus) of the EBA and the supramarginal gyrus showed greater sensitivity to recognized hand shapes than to inanimate objects, regardless of the sensory modality and visual experience. Unlike the superior part of the EBA, the sensitivity of the inferior part (i.e., the inferior temporal sulcus and middle occipital gyrus) depended on visual experience. However, this vision-dependent sensitivity explained minor individual differences in hand-recognition performance. These results indicate that nonvisual modalities drive the development of the cortical network underlying the recognition of hand gestures with a node in the visual cortex.

Functional relevance of the extrastriate body area for visual and haptic object recognition: a preregistered fMRI-guided TMS study.

The extrastriate body area (EBA) is a region in the lateral occipito-temporal cortex (LOTC), which is sensitive to perceived body parts. Neuroimaging studies suggested that EBA is related to body and tool processing, regardless of the sensory modalities. However, how essential this region is for visual tool processing and nonvisual object processing remains a matter of controversy. In this preregistered fMRI-guided repetitive transcranial magnetic stimulation (rTMS) study, we examined the causal involvement of EBA in multisensory body and tool recognition. Participants used either vision or haptics to identify 3 object categories: hands, teapots (tools), and cars (control objects). Continuous theta-burst stimulation (cTBS) was applied over left EBA, right EBA, or vertex (control site). Performance for visually perceived hands and teapots (relative to cars) was more strongly disrupted by cTBS over left EBA than over the vertex, whereas no such object-specific effect was observed in haptics. The simulation of the induced electric fields confirmed that the cTBS affected regions including EBA. These results indicate that the LOTC is functionally relevant for visual hand and tool processing, whereas the rTMS over EBA may differently affect object recognition between the 2 sensory modalities.

The Effect of Temperature on Tactile Softness Perception.

We are adept at discriminating object properties such as softness and temperature using touch. Previous studies have investigated the nature of each object property, but the interactions between these properties are not fully understood. Tactile softness perception relies on multiple sensory cues such as the size of the contact area, indentation depth, and force exerted. In addition to these cues, the temperature of the stimulus may contribute to tactile softness perception by changing the sensitivity to changes in stimulus compliance. To test this hypothesis, we conducted two psychophysical experiments in which the subjects estimated the magnitude of perceived softness after touching deformable objects. We varied the compliance and temperature of the stimuli. The linear functions of compliance fit to the magnitude estimates under cold conditions (9-15°C) were steeper than the functions fit to the magnitude estimates under room temperature (21-25°C). These results indicate that temperature can sharpen our tactile softness perception of deformable surfaces by increasing the sensitivity to differences in compliance.

Japanese Sound-Symbolic Words for Representing the Hardness of an Object Are Judged Similarly by Japanese and English Speakers.

Contrary to the assumption of arbitrariness in modern linguistics, sound symbolism, which is the non-arbitrary relationship between sounds and meanings, exists. Sound symbolism, including the "Bouba-Kiki" effect, implies the universality of such relationships; individuals from different cultural and linguistic backgrounds can similarly relate sound-symbolic words to referents, although the extent of these similarities remains to be fully understood. Here, we examined if subjects from different countries could similarly infer the surface texture properties from words that sound-symbolically represent hardness in Japanese. We prepared Japanese sound-symbolic words of which novelty was manipulated by a genetic algorithm (GA). Japanese speakers in Japan and English speakers in both Singapore and the United States rated these words based on surface texture properties (hardness, warmness, and roughness), as well as familiarity. The results show that hardness-related words were rated as harder and rougher than softness-related words, regardless of novelty and countries. Multivariate analyses of the ratings classified the hardness-related words along the hardness-softness dimension at over 80% accuracy, regardless of country. Multiple regression analyses revealed that the number of speech sounds /g/ and /k/ predicted the ratings of the surface texture properties in non-Japanese countries, suggesting a systematic relationship between phonetic features of a word and perceptual quality represented by the word across culturally and linguistically diverse samples.

Identification and Quantitation of Taste-Active Compounds in Dried Scallops by Combined Application of the Sensomics and a Quantitative NMR Approach.

Application of the sensomics concept on dried scallops, a Japanese specialty produced from the adductor muscle of scallops, revealed after activity-guided fractionation with subsequent (comparative) taste dilution analyses besides nucleotides, amino acids, organic acids, and inorganic ions, the presence of taste-modulating quaternary ammonium compounds and opines in highly taste-active fractions. In order to recreate the taste of dried scallops, two independent quantitation approaches were applied and compared. The first approach used multiple targeted UHPLC-MS/MS and high-performance ion chromatography methods. Besides already established quantitation methods for basic taste compounds, a new HILIC-UHPLC-MS/MSMRM method for the quantitation of chromatographically challenging opines, using synthesized stable isotope-labeled standards, was developed. Furthermore, a qHNMR approach was applied, enabling a direct identification and quantitation of organic taste compounds in a food extract without prior fractionation using a reference 1H NMR database. Both methods yielded similar quantitative results of taste-active compounds in dried scallop extracts and subsequent taste recombination experiments based on these data were able to recreate the taste of dried scallops.

Coexistence of sensory qualities and value representations in human orbitofrontal cortex.

Despite the multiple regions and neural networks associated with value-based decision-making, the orbitofrontal cortex (OFC) is possible a particularly important one. Although the role of the OFC in reinforcer devaluation tasks, which assess the ability to represent identity, sensory qualities, and subjective values of the expected outcomes, has been established, the specific aspect represented in this area remains unclear. In this study, using functional magnetic resonance imaging, wherein participants rated the palatability of 128 food items using photographs, we investigated whether the human OFC represents object identity, sensory qualities, or value. Employing many items helped us dissociate object identity from sensory qualities and values; the inferred sensory qualities of identical items were manipulated by a change in metabolic state. Moreover, value differences between items were analytically controlled by employing a technique similar to age adjustment. The palatability ratings for food items significantly decreased after a meal. Using representational similarity analysis, we confirmed that the OFC represents value. Moreover, identical items were represented similarly in the lateral OFC in a given metabolic state; however, these representations were altered post-feeding. Importantly, this change was not explained by subjective value, suggesting that the OFC represents sensory quality and value, but not object identity.

Nerve and behavioral responses of mice to various umami substances.

Food contains various taste substances. Among them, umami substances play an important role with regard to the perception of the taste of food, but, few studies have examined the taste characteristics of representative umami substances other than monosodium L-glutamate (MSG). By conducting mouse behavioral studies (the 48-h 2-bottle preference test and the conditioned taste aversion test) and assessing gustatory nerve responses, we investigated the taste characteristics of unique umami substances, including sodium succinate, L-theanine, betaine, and the enantiomer of MSG, D-MSG. Furthermore, we examined the synergy of umami with inosine 5'-monophoshate (IMP). In the case of the mice, sodium succinate had an umami taste and showed strong synergy with IMP. L-theanine showed synergy with IMP but did not have an umami taste without IMP. In contrast, betaine did not have an umami taste or synergy with IMP. D-MSG might have weak synergy with IMP.

Physical correlates of human-like softness elicit high tactile pleasantness.

Touching an object can elicit affective sensations. Because these sensations are critical for social interaction, tactile preferences may be adapted to the characteristics of the human body. We have previously shown that compliance, a physical correlate of softness, increased the tactile pleasantness of a deformable surface. However, the extent to which object compliance similar to the human body elicits tactile pleasantness remains unknown. We addressed this question by using a wide range of compliances and by measuring the distribution of compliance of human body parts. The participants numerically estimated the perceived pleasantness or softness while pushing tactile stimuli with their right index fingers. The perceived softness monotonically increased with increasing compliance and then leveled off around the end of the stimulus range. By contrast, pleasantness showed an inverse U pattern as a function of compliance, reaching the maximum between 5 and 7 mm/N. This range of compliance was within that for both hand and arm. These results indicate that objects with similar compliance levels as those of human body parts yield the highest pleasantness when pushing them.

Brain networks underlying the processing of sound symbolism related to softness perception.

Unlike the assumption of modern linguistics, there is non-arbitrary association between sound and meaning in sound symbolic words. Neuroimaging studies have suggested the unique contribution of the superior temporal sulcus to the processing of sound symbolism. However, because these findings are limited to the mapping between sound symbolism and visually presented objects, the processing of sound symbolic information may also involve the sensory-modality dependent mechanisms. Here, we conducted a functional magnetic resonance imaging experiment to test whether the brain regions engaged in the tactile processing of object properties are also involved in mapping sound symbolic information with tactually perceived object properties. Thirty-two healthy subjects conducted a matching task in which they judged the congruency between softness perceived by touch and softness associated with sound symbolic words. Congruency effect was observed in the orbitofrontal cortex, inferior frontal gyrus, insula, medial superior frontal gyrus, cingulate gyrus, and cerebellum. This effect in the insula and medial superior frontal gyri was overlapped with softness-related activity that was separately measured in the same subjects in the tactile experiment. These results indicate that the insula and medial superior frontal gyrus play a role in processing sound symbolic information and relating it to the tactile softness information.

The extrastriate body area is involved in reciprocal imitation of hand gestures, vocalizations, and facial expressions: A univariate and multivariate fMRI study.

The extrastriate body area (EBA) in the lateral occipito-temporal cortex has an important role in reciprocal interaction, as it detects congruence between self and other's hand actions. However, it is unclear whether the EBA can detect congruence regardless of the type of action. In the present study, we examined the neural substrate underlying congruence detection of three types of actions: hand gestures, vocalizations, and facial expressions. A univariate analysis revealed a congruency effect, especially for imitating action, for all three types of actions in the EBA. A multi-voxel pattern analysis classifier in the EBA was able to distinguish between initiating interaction from responding to interaction in all experiments. Correspondingly, the congruency effect in the EBA revealed by univariate analysis was stronger for responding to than for initiating interaction. These findings suggest that the EBA might contribute to detect congruence regardless of the body part used (i.e. face or hand) and the type of action (i.e. gestural or vocal). Moreover, initiating and responding to interaction might be processed differently within the EBA. This study highlights the role of the EBA in comparing between self and other's actions beyond hand actions.Running head: Function of EBA in reciprocal imitation.

Brain networks involved in haptic and visual identification of facial expressions of emotion: an fMRI study.

Previous neurophysiological and neuroimaging studies have shown that a cortical network involving the inferior frontal gyrus (IFG), inferior parietal lobe (IPL) and cortical areas in and around the posterior superior temporal sulcus (pSTS) region is employed in action understanding by vision and audition. However, the brain regions that are involved in action understanding by touch are unknown. Lederman et al. (2007) recently demonstrated that humans can haptically recognize facial expressions of emotion (FEE) surprisingly well. Here, we report a functional magnetic resonance imaging (fMRI) study in which we test the hypothesis that the IFG, IPL and pSTS regions are involved in haptic, as well as visual, FEE identification. Twenty subjects haptically or visually identified facemasks with three different FEEs (disgust, neutral and happiness) and casts of shoes (shoes) of three different types. The left posterior middle temporal gyrus, IPL, IFG and bilateral precentral gyrus were activated by FEE identification relative to that of shoes, regardless of sensory modality. By contrast, an inferomedial part of the left superior parietal lobule was activated by haptic, but not visual, FEE identification. Other brain regions, including the lingual gyrus and superior frontal gyrus, were activated by visual identification of FEEs, relative to haptic identification of FEEs. These results suggest that haptic and visual FEE identification rely on distinct but overlapping neural substrates including the IFG, IPL and pSTS region.

The Effect of Object Compliance on the Velvet Hand Illusion.

Movement of a grid of bars between the two hands creates the tactile illusion of a velvet-like material, namely, the velvet hand illusion (VHI). It was recently proposed that the VHI is caused by a masking effect; bar movement suppresses conscious perception of tactile inputs from the opposing hand. If this hypothesis sufficiently explains the VHI, the physical properties of the opposing hand should not affect the illusion. Another hypothesis suggests that the integration of inputs from the grid of bars and the hands plays a critical role in the VHI. To compare these two hypotheses, the VHI was elicited under two conditions; the grid of bars was between one hand and a soft texture or the grid of bars was between one hand and a hard texture. A hand was stimulated by moving bars while contacting the stationary texture held by the opposing hand. The grid of bars with the soft texture induced a stronger illusion and softer feeling than that with the hard texture. This result supports the integration hypothesis in which tactile inputs from both bars and textures attached to the opposing hand are integrated.

Tactile perception of pleasantness in relation to perceived softness.

The sense of touch allows us to infer objects' physical properties, while the same input also produces affective sensations. These affective sensations are important for interpersonal relationships and personal well-being, which raises the possibility that tactile preferences are adapted to the characteristics of the skin. Previous studies examined how physical properties such as surface roughness and temperature influence affective sensations; however, little is known about the effect of compliance (physical correlate of softness) on pleasantness. Thus, we investigated the psychophysical link between softness and pleasantness. Pieces of human skin-like rubber with different compliances were pressed against participants' fingers. Two groups of participants numerically estimated the perceived magnitude of either pleasantness or softness. The perceived magnitude of pleasantness and softness both increased monotonically as a function of increasing object compliance, levelling off at around the end of the stimulus range. However, inter-subject variability was greater for pleasantness than for perceived softness, whereas the slope of the linear function fit to the magnitude estimates was steeper for softness than for pleasantness. These results indicate that object compliance is a critical physical determinant for pleasantness, whereas the effect of compliance on pleasantness was more variable among individuals than the effect on softness was.

Differences between children and adults in functional connectivity between the inferior frontal gyrus and extrastriate body area for gestural interaction.

Gestural interaction, where a person initiates interaction (initiator) and another person responds to it (follower), changes during development. The neural network comprising the inferior frontal gyrus (IFG), inferior parietal lobule (IPL), and the lateral occipito-temporal cortex (LOTC) is relevant to gestural interaction. The LOTC includes the extrastriate body area (EBA). Activation of these brain regions depends on the initiating/following role in adults. We conducted functional magnetic resonance imaging study on 18 children and 18 adults, to elucidate developmental changes of the neural mechanism underlying gestural interaction. We manipulated the initiating/following role (initiating/following) and congruency (congruent/incongruent) of executed and observed actions. After analyzing regional brain activity, we assessed psycho-physiological interaction to examine functional connectivity. Activation in the IFG and connectivity between the IFG and EBA in the Initiating rather than Following condition, which might be associated with evaluating social relevance, was stronger in adults than in children. The increase of the incongruency effect in the following condition (relative to the initiating condition) in the bilateral IPL was significantly attenuated in children compared with adults. These results suggest that the fronto-parieto-temporal network, involved in gestural interactions, undergoes developmental changes.

Visual Body Part Representation in the Lateral Occipitotemporal Cortex in Children/Adolescents and Adults.

The lateral occipitotemporal cortex (LOTC) that responds to human bodies and body parts has been implicated in social development and neurodevelopmental disorders like autism spectrum disorder (ASD). Neuroimaging studies using a representational similarity analysis (RSA) revealed that body representation in the LOTC of typically developing (TD) adults is categorized into 3 clusters: action effector body parts, noneffector body parts, and face parts. However, its organization of younger people (i.e., children and adolescents) and its association with individual traits remain unclear. In this functional MRI study, TD adults and children/adolescents observed photographs of hands, feet, arms, legs, chests, waists, upper/lower faces, the whole body, and chairs. The univariate analysis showed that fewer child/adolescent participants showed left LOTC activation in response to whole-body images (relative to those of chairs) than adult participants. Contrastingly, the RSA on both age groups revealed a comparable body representation with 3 clusters of body parts in the bilateral LOTC. Hence, this result indicates that, although response to whole-body images can differ, LOTC body part representations for children/ adolescents and adults are highly similar. Furthermore, sensory atypicality is associated with spatial LOTC organization, suggesting the importance of this region for understanding individual difference, which is frequently observed in ASD.

Emotional Tears Communicate Sadness but Not Excessive Emotions Without Other Contextual Knowledge.

Contexts of face perception are diverse. They range from the social environment to body postures, from the expresser's gaze direction to the tone of voice. In extending the research on contexts of face perception, we investigated people's perception of tears on a face. The act of shedding tears is often perceived as an expression of sad feelings aroused by experiencing loss, disappointment, or helplessness. Alternatively, tears may also represent the excessive intensity of any emotion, such as extreme fear during an unexpected encounter with a giant bear and extreme happiness when you win a competition. Investigating these competing interpretations of tears, we found that the addition of tears to different facial expressions made the expressions conceptually closer to sad expressions. In particular, the results of the similarity analysis showed that, after the addition of tears, patterns of ratings for anger, fear, disgust, and neutral facial expressions became more similar to those for sadness expressions. The effect of tears on the ratings of basic emotions and their patterns in facial expressions are discussed.

Affective judgement of social touch on a hand associated with hand embodiment.

Social touch constitutes a critical component of human interactions. A gentle tap on the hand, for instance, can sometimes create emotional bonding and reduce interpersonal distance in social interactions. Evidence of tactile empathy suggests that touch can be experienced through both physical sensation and observation, yet vicarious perception of observed touch on an object as a function of the object's conceptual representation (e.g., Is this object identified as mine? Does this object feel like part of me?) remains less explored. Here we examined the affective judgement of social touch when the illusory sense of ownership over a dummy hand was manipulated through the rubber-hand illusion. When the same social touch was performed on either the real or the dummy hand, we found a similar sense of perceived pleasantness between the felt and observed touch, but only when the dummy hand was embodied; when it was not, the perceived pleasantness of the observed touch was lesser (an "embodiment effect"; Experiment 1). In addition, we found that the embodiment effect associated with the observed touch was insensitive to the way in which embodiment was manipulated (Experiment 2), and that this effect was specific to social but not neutral touch (Experiment 3). Taken together, our findings suggest a role of embodiment in the affective component of observed social touch and contribute to our understanding of tactile empathy for objects.